The First Cytokine Sequence Within Cartilaginous Fish

IL-1β in the Small Spotted Catshark (Scyliorhinus canicula)

Steven Bird, Tiehui Wang, Jun Zou, C Cunningham, Christopher John Secombes

Research output: Contribution to journalArticle

88 Citations (Scopus)

Abstract

Cartilaginous fish are considered the most primitive living jawed vertebrates with a complex immune system typical of all jawed vertebrates. Cytokine homologs are found within jawless and bony fish, although no cytokine or cytokine receptor genes have been sequenced in cartilaginous fish. In this study the complete coding sequence of the small spotted catshark (Scyliorhinus canicula) IL-1beta gene is presented that contains a short 5' untranslated region (54 bp), a 903-bp open reading frame, a 379-bp 3' untranslated region, a polyadenylation signal, and eight mRNA instability motifs. The predicted translation (301 amino acids) has highest identity to trout IL-1beta (31.7%), with greatest homology within the putative 12 beta-sheets. The IL-1 family signature is also present, but there is no apparent signal peptide. As with other nonmammalian IL-1beta sequences, the IL-1-converting enzyme cut site is absent. Expression of the IL-1beta transcript is detectable by RT-PCR in the spleen and testes, induced in vivo with LPS. Furthermore, a 7-fold increase of transcript levels in splenocytes incubated for 5 h with LPS was seen. The genomic organization comprises six exons and five introns with highest homology seen in exons encoding the largest amount of secondary structure per amino acid. Southern blot analysis suggests at least two copies of the IL-1beta gene or genes related to the 3' end of the IL-1beta sequence are present in the catshark. The cloning of IL-1beta in S. canicula, the first cytokine sequenced within cartilaginous fish, verifies previous bioactivity evidence for the presence of inflammatory cytokines.
Original languageEnglish
Pages (from-to)3329-3340
Number of pages12
JournalThe Journal of Immunology
Volume168
Issue number7
DOIs
Publication statusPublished - 1 Apr 2002

Keywords

  • Amino Acid Sequence
  • Animals
  • Base Sequence
  • Blotting, Southern
  • Cloning, Molecular
  • Exons
  • Gene Expression
  • Humans
  • Interleukin-1
  • Introns
  • Male
  • Mice
  • Molecular Sequence Data
  • Organ Specificity
  • Sequence Alignment
  • Sequence Analysis, DNA
  • Sequence Analysis, Protein
  • Sequence Homology, Amino Acid
  • Sharks
  • Trout Onchorhynchus-Mykiss
  • Growth-Factor-Beta
  • Interleukin-1-beta Gene
  • Expression
  • Cloning
  • Identification
  • Protein
  • Shark
  • Organization
  • Leukocytes

Cite this

The First Cytokine Sequence Within Cartilaginous Fish : IL-1β in the Small Spotted Catshark (Scyliorhinus canicula). / Bird, Steven; Wang, Tiehui; Zou, Jun; Cunningham, C ; Secombes, Christopher John.

In: The Journal of Immunology, Vol. 168, No. 7, 01.04.2002, p. 3329-3340.

Research output: Contribution to journalArticle

@article{5d8658f1f4c2411f8e6a6e83e4bbf345,
title = "The First Cytokine Sequence Within Cartilaginous Fish: IL-1β in the Small Spotted Catshark (Scyliorhinus canicula)",
abstract = "Cartilaginous fish are considered the most primitive living jawed vertebrates with a complex immune system typical of all jawed vertebrates. Cytokine homologs are found within jawless and bony fish, although no cytokine or cytokine receptor genes have been sequenced in cartilaginous fish. In this study the complete coding sequence of the small spotted catshark (Scyliorhinus canicula) IL-1beta gene is presented that contains a short 5' untranslated region (54 bp), a 903-bp open reading frame, a 379-bp 3' untranslated region, a polyadenylation signal, and eight mRNA instability motifs. The predicted translation (301 amino acids) has highest identity to trout IL-1beta (31.7{\%}), with greatest homology within the putative 12 beta-sheets. The IL-1 family signature is also present, but there is no apparent signal peptide. As with other nonmammalian IL-1beta sequences, the IL-1-converting enzyme cut site is absent. Expression of the IL-1beta transcript is detectable by RT-PCR in the spleen and testes, induced in vivo with LPS. Furthermore, a 7-fold increase of transcript levels in splenocytes incubated for 5 h with LPS was seen. The genomic organization comprises six exons and five introns with highest homology seen in exons encoding the largest amount of secondary structure per amino acid. Southern blot analysis suggests at least two copies of the IL-1beta gene or genes related to the 3' end of the IL-1beta sequence are present in the catshark. The cloning of IL-1beta in S. canicula, the first cytokine sequenced within cartilaginous fish, verifies previous bioactivity evidence for the presence of inflammatory cytokines.",
keywords = "Amino Acid Sequence, Animals, Base Sequence, Blotting, Southern, Cloning, Molecular, Exons, Gene Expression, Humans, Interleukin-1, Introns, Male, Mice, Molecular Sequence Data, Organ Specificity, Sequence Alignment, Sequence Analysis, DNA, Sequence Analysis, Protein, Sequence Homology, Amino Acid, Sharks, Trout Onchorhynchus-Mykiss, Growth-Factor-Beta, Interleukin-1-beta Gene , Expression , Cloning, Identification, Protein, Shark, Organization, Leukocytes",
author = "Steven Bird and Tiehui Wang and Jun Zou and C Cunningham and Secombes, {Christopher John}",
year = "2002",
month = "4",
day = "1",
doi = "10.4049/jimmunol.168.7.3329",
language = "English",
volume = "168",
pages = "3329--3340",
journal = "The Journal of Immunology",
issn = "0022-1767",
publisher = "American Association of Immunologists",
number = "7",

}

TY - JOUR

T1 - The First Cytokine Sequence Within Cartilaginous Fish

T2 - IL-1β in the Small Spotted Catshark (Scyliorhinus canicula)

AU - Bird, Steven

AU - Wang, Tiehui

AU - Zou, Jun

AU - Cunningham, C

AU - Secombes, Christopher John

PY - 2002/4/1

Y1 - 2002/4/1

N2 - Cartilaginous fish are considered the most primitive living jawed vertebrates with a complex immune system typical of all jawed vertebrates. Cytokine homologs are found within jawless and bony fish, although no cytokine or cytokine receptor genes have been sequenced in cartilaginous fish. In this study the complete coding sequence of the small spotted catshark (Scyliorhinus canicula) IL-1beta gene is presented that contains a short 5' untranslated region (54 bp), a 903-bp open reading frame, a 379-bp 3' untranslated region, a polyadenylation signal, and eight mRNA instability motifs. The predicted translation (301 amino acids) has highest identity to trout IL-1beta (31.7%), with greatest homology within the putative 12 beta-sheets. The IL-1 family signature is also present, but there is no apparent signal peptide. As with other nonmammalian IL-1beta sequences, the IL-1-converting enzyme cut site is absent. Expression of the IL-1beta transcript is detectable by RT-PCR in the spleen and testes, induced in vivo with LPS. Furthermore, a 7-fold increase of transcript levels in splenocytes incubated for 5 h with LPS was seen. The genomic organization comprises six exons and five introns with highest homology seen in exons encoding the largest amount of secondary structure per amino acid. Southern blot analysis suggests at least two copies of the IL-1beta gene or genes related to the 3' end of the IL-1beta sequence are present in the catshark. The cloning of IL-1beta in S. canicula, the first cytokine sequenced within cartilaginous fish, verifies previous bioactivity evidence for the presence of inflammatory cytokines.

AB - Cartilaginous fish are considered the most primitive living jawed vertebrates with a complex immune system typical of all jawed vertebrates. Cytokine homologs are found within jawless and bony fish, although no cytokine or cytokine receptor genes have been sequenced in cartilaginous fish. In this study the complete coding sequence of the small spotted catshark (Scyliorhinus canicula) IL-1beta gene is presented that contains a short 5' untranslated region (54 bp), a 903-bp open reading frame, a 379-bp 3' untranslated region, a polyadenylation signal, and eight mRNA instability motifs. The predicted translation (301 amino acids) has highest identity to trout IL-1beta (31.7%), with greatest homology within the putative 12 beta-sheets. The IL-1 family signature is also present, but there is no apparent signal peptide. As with other nonmammalian IL-1beta sequences, the IL-1-converting enzyme cut site is absent. Expression of the IL-1beta transcript is detectable by RT-PCR in the spleen and testes, induced in vivo with LPS. Furthermore, a 7-fold increase of transcript levels in splenocytes incubated for 5 h with LPS was seen. The genomic organization comprises six exons and five introns with highest homology seen in exons encoding the largest amount of secondary structure per amino acid. Southern blot analysis suggests at least two copies of the IL-1beta gene or genes related to the 3' end of the IL-1beta sequence are present in the catshark. The cloning of IL-1beta in S. canicula, the first cytokine sequenced within cartilaginous fish, verifies previous bioactivity evidence for the presence of inflammatory cytokines.

KW - Amino Acid Sequence

KW - Animals

KW - Base Sequence

KW - Blotting, Southern

KW - Cloning, Molecular

KW - Exons

KW - Gene Expression

KW - Humans

KW - Interleukin-1

KW - Introns

KW - Male

KW - Mice

KW - Molecular Sequence Data

KW - Organ Specificity

KW - Sequence Alignment

KW - Sequence Analysis, DNA

KW - Sequence Analysis, Protein

KW - Sequence Homology, Amino Acid

KW - Sharks

KW - Trout Onchorhynchus-Mykiss

KW - Growth-Factor-Beta

KW - Interleukin-1-beta Gene

KW - Expression

KW - Cloning

KW - Identification

KW - Protein

KW - Shark

KW - Organization

KW - Leukocytes

U2 - 10.4049/jimmunol.168.7.3329

DO - 10.4049/jimmunol.168.7.3329

M3 - Article

VL - 168

SP - 3329

EP - 3340

JO - The Journal of Immunology

JF - The Journal of Immunology

SN - 0022-1767

IS - 7

ER -